Lachryphagy by cockroaches: reptile tears to increase reproductive output?

ABSTRACT

Lachryphagy, or tear-feeding, is generally considered as supplementary feeding by invertebrates with a long proboscis to acquire essential nutrients. Commonly reported vertebrate host species of lachrypaghic interations are humans and birds, and in reptiles concern large species: turtles and crocodiles, with one report from an iguanid host. Here, we report tear-feeding by a cockroach, a species lacking a proboscis, on a small squamate species, Anolis fuscoauratus. We address how the nutritional needs for the reproductive cycle may force cockroaches to explore any dietary source with essential nutrients. In addition to birds, our report adds Anolis as invertebrate predators that are visited by lachryphagous invertebrates, interactions that may be restricted to nights to reduce predation risk for the feeding invertebrates. This report extends tear-feeding behavior to proboscis-lacking invertebrates, and to small squamate hosts, and demonstrates that lachryphagy on reptilian hosts is not restricted to diurnal occurrence. Overall, this observation suggests that similar interactions could be far more frequent.

KEYWORDS:

• Amazon
• Anolis
• nocturnal
• reptilian
• South America
• species interaction
• squamata
• tear-feeding

During the night of 29 March 2019, JAGR observed a sleeping Anolis fuscoauratus D’Orbigny, 1837, with a cockroach positioned on its head, on a branch within a close-canopy forest near Rio Curaray in the Ecuadorian Amazon (Figure 1; −1.66850, −75.93606; 200 m elevation). While observing from a distance (~3 m) to not disturb the interaction, the cockroach (Amazonica or Cariblatta sp.; L. Vidlička and S. Lopes pers. comm.) remained motionless for several minutes with its mouth placed over the corner of the anoles’ eye, presumably feeding on (secreted) tear fluid, known as lachryphagy. Upon approaching to photograph the interaction, the cockroach had moved slightly away from the eye, and the anole opened its eyes but remained immobile as it did throughout the observation, seemingly undisturbed by the cockroach. We are unaware of tear-feeding Blattaria (cockroaches) reports or lachryphagy with anole lizards as hosts.

Figure 1. Cockroach positioned on head of Anolis fuscoauratus, on 29 March 2019 in the Ecuadorian Amazon

Puddling is considered as the supplementary feeding on moist ground, carcasses, excrements or secretions of vertebrates, such as tears [1,2]. Reports of lachryphagy are mainly from butterflies and moths, though other entomological groups also engage in such interactions, including species that lack a long proboscis (e.g. in Hymenoptera [1,3–5]). Through this biotic, seemingly commensalism, interaction, feeders are believed to acquire essential minerals and proteins from a range of host species, including humans, birds, turtles, crocodiles, and even a recent report of an iguanid [6–8]. Interestingly, tears have recently been shown to include urea as well as proteins and glucose in a range of species, including reptiles and birds [9].

Efficient acquisition of key resources is important to avoid nutrient deficiency hampering reproduction in herbivorous invertebrates [2,5]. Finding nutrient-rich resources is essential to optimize fitness, but is challenging in biodiverse, highly competitive ecosystems with fast nutrient cycling, like tropical rainforests. In addition to phosphorous and sodium [10], supplemental uptake of nitrogen is often mentioned to drive puddling behavior [2]. In the species-rich Blattaria, completion of the reproduction cycle depends on the uptake of phosphorus- or nitrogen-rich food sources [11]; and the uptake of uric acid has received extensive scientific interest. Nitrogen content allocated to uric acid can increase by 27-fold during the reproduction cycle of numerous Blattaria species [11].

High demand for uric acid has contributed to mating systems where male cockroaches aid females with uric acid acquisition, which occurs in multiple Blattaria subfamilies [12,13]. Males are known to aid females by covering sperm packages with uric acid or providing it as a dietary source from a special gland, directly after copulation [12,13]. As females can mate repeatedly, by supplementing uric acid, males increase their own reproductive output as it decreases the timeframe between copulation and oviposition by the female. Both sexes need uric acid sources to increase reproductive output and complete their reproductive cycle, which may be as short as 7 days in some species [14].

Cockroaches are under strong fitness pressure to locate and feed on key dietary sources to complete their reproduction cycle. Despite our 50-year understanding of cockroach reproduction, in-situ resources seem not often reported, e.g. leaf litter, algae, fruits, bark, guano and bird and reptile droppings [11,14,15]. Our observation extends this to tears, known to include urea as well as proteins and glucose [9]. Fitness pressure may induce the risky behavior of lachryphagy by the cockroach. Contrary to lachryphagous feeders with a long proboscis [16], species lacking a proboscis could risk harm or predation as they are near the host’ head. Some diurnal reptiles may be active during nights, close to full moon conditions, including Anolis [17]. Future observations will enable us to better understand these interactions and their occurrence.

The importance of our observation is three-fold by extending tear-feeding behavior to cockroaches and to small squamate hosts and showing that lachryphagy on reptilian hosts is not restricted to diurnal occurrence. Interestingly, diurnal reports of lachryphagy mainly include large hosts (turtles and crocodiles), while small hosts are reported for nocturnal observations. As birds and anoles are important invertebrate predators, nocturnal lachryphagous feeding by invertebrates presumably lowers predation risk. Furthermore, as Amazonian reptilians and cockroaches are extremely diverse and abundant [18–21] similar interactions could be far more frequent. Future observations and studies are thus expected to explore how lachryphagic interactions occur in other invertebrates and vertebrate hosts.

Observing interactions as those reported here is time-consuming and difficult to collect data on, i.e. they occur in remote places, can occur during the night, and last short periods of time. As images are widely being shared on public online community-science platforms (e.g. iNaturalist) and in species-dedicated social media groups [22], these may aid collaborations between scientists and non-scientists to further our understanding of the natural world. Equal to more traditional information sources, scientists should familiarize themselves with online public platforms and social media platforms that may provide data on their study species.

Acknowledgments

We thank Lubomir Vidlička and Sonia Lopes for species identification of the cockroach, as well as two anonymous reviewers for their helpful comments that improved this manuscript. We are thankful to the community of Lorocachi for providing accommodations, food and their help during our stay and specifically to Gonzalo Nazati Vela for his invaluable help during this and previous expeditions.

Disclosure statement

No potential conflict of interest was reported by the author(s).